Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries)

Zhao, Xingbo; Li, N; Guo, Weiwei; Hu, Xiaoxiang; Liu, Z; Gong, Guochun; Wang, A; Feng, Juan; Wu, Changxin

doi:10.1038/sj.hdy.6800516

Cited by 101 publications

(49 citation statements)

References 22 publications

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“…4A-D), opinions may vary as to whether the same holds true for sperm mtDNA. Some population studies defend the possibility of paternal-maternal mtDNA recombination after sperm mtDNA leakage (Awadalla et al, 1999;Eyre-Walker et al, 1999;Hagelberg, 1999a;Zhao et al, 2001) and it is yet to be demonstrated that the degradation of sperm mitochondrial proteins is parallel to the hydrolysis of sperm mtDNA. It should be considered that the sperm mitochondria can survive inside other cells (Manfredi et al, 1997).…”

Section: Evolutionary Considerationsmentioning

confidence: 98%

Ubiquitin‐dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: Killing three birds with one stone

Šutovský

2003

Microscopy Res & Technique

254

181

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Ubiquitin and ubiquitin-like proteins control the degradation of substrates as diverse as cyclins, viral envelope proteins, plasma membrane receptors, and mRNAs. The ubiquitinated substrates are targeted towards the lysosomal or proteasomal degradation sites. The number and position of ubiquitin molecules bound to substrates' lysine residues and the number and position of ubiquitin molecules in polyubiquitin chains determine the astonishing substrate specificity of ubiquitin-mediated proteolysis. Ubiquitin is likely to be expressed in mammalian gametes and embryos at any given developmental step, but the information on ubiquitin dependence of gametogenesis and fertilization is sketchy. Ubiquitin ligases E1, E2, E3, and UBC4 are active in the testis. Ubiquitin and proteasomal subunits can be detected in the human sperm centrosome that undergoes dramatic reduction during spermatid elongation. Spermatid histones are ubiquitinated as they are being transiently replaced by transitional proteins and permanently by protamines. Ubiquitin tagging of the sperm mitochondrial membranes may serve as a death sentence for paternal mitochondria at fertilization, thus promoting the maternal inheritance of mitochondrial DNA (mtDNA) in mammals. The defective spermatozoa become surface-ubiquitinated during sperm descent down the epididymis. Finally, new evidence suggests the involvement of ubiquitin-proteasome pathway in the zona penetration by the acrosome-reacted spermatozoon. Such differential patterns of ubiquitination in the testis and epididymis, and inside the egg, may be necessary for reproductive success in humans and animals. Deciphering and eventually manipulating the ubiquitin-dependent proteolysis in the reproductive system could allow us to redirect the mode of mtDNA inheritance after cloning and ooplasmic transplantation, provide germ line therapy in some cases of male infertility, develop new contraceptives, manage polyspermia during in vitro fertilization, and establish objective markers for infertility diagnostics, semen evaluation, and prediction of future fertility.

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Section: Evolutionary Considerationsmentioning

confidence: 98%

Ubiquitin‐dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: Killing three birds with one stone

Šutovský

2003

Microscopy Res & Technique

254

181

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“…However, it was recently shown in a patient with mitochondrial myopathy that the pathogenic mtDNA was of paternal origin (Schwartz and Vissing, 2002). Evidence for the occasional paternal transmission of mtDNA has also been reported in sheep, mice, cattle, mussels, and insects (Zhao et al, 2004). Although rare, the paternal inheritance of mtDNA may have a significant impact on evolution and on disease development.…”

Section: Mitochondrial Dna Inheritancementioning

confidence: 99%

Mitochondrial genetics

Lemire¹

2005

WormBook

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“…Organisms such as the blue mussel (Cogswell et al, 2006) and Chlamydomonas (Aoyama et al, 2006) inherit paternal mitochondria but most mammals inherit mitochondria and mtDNA maternally (Kuroiwa, 1991;Birky, 1995), with paternal mitochondrial inheritance being a rare event, as proposed in sheep (Zhao et al, 2004). Early theories attempted to explain maternal mtDNA inheritance by the dilution of paternal mtDNA in the oocyte (Hecht et al, 1984;Jansen and de Boer, 1998;Birky, 2001;Diez-Sanchez et al, 2003).…”

mentioning

confidence: 95%

Expression of mitochondrial transcription factor A (TFAM) during porcine gametogenesis and preimplantation embryo development

Antelman

Manandhar

et al. 2008

Journal Cellular Physiology

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Mitochondrial transcription factor A (TFAM) is responsible for stability, maintenance, and transcriptional control of mitochondrial DNA (mtDNA). We have studied the expression and distribution of TFAM in the gametes and preimplantation embryos of the domestic pig (Sus scrofa). We hypothesized that TFAM is not present in the boar sperm mitochondria to reduce the possibility of paternal mtDNA propagation in the progeny. In contrast, we anticipated that Tfam gene is expressed in a developmental stage-dependent manner in porcine oocytes and embryos. The appropriate TFAM band of 25 kDa was detected by Western blotting in ejaculated boar spermatozoa, as well as in porcine oocytes and zygotes. Boar sperm extracts also displayed several bands >25 kDa suggestive of post-translational modification by ubiquitination, confirmed by affinity purification of ubiquitinated proteins. TFAM immunoreactivity was relegated to the sperm tail principal piece and sperm head in fully differentiated spermatozoa. The content of Tfam mRNA increased considerably from the germinal vesicle to blastocyst stage and also between in vitro fertilized and cultured blastocysts compared to in vivo-derived blastocysts. TFAM protein accumulated in the oocytes during maturation and was reduced by proteolysis after fertilization. This pattern was not mirrored in parthenogenetically activated oocytes and zygotes reconstructed by SCNT, suggesting deviant processing of TFAM protein and transcript after oocyte/embryo manipulation. Thus, TFAM may exert a critical role in porcine gametogenesis and preimplantation embryo development. Altogether, our data on the role of TFAM in mitochondrial function and inheritance have broad implications for cell physiology and evolutionary biology.

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Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries)

Cited by 101 publications

References 22 publications

Ubiquitin‐dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: Killing three birds with one stone

Ubiquitin‐dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: Killing three birds with one stone

Mitochondrial genetics

Expression of mitochondrial transcription factor A (TFAM) during porcine gametogenesis and preimplantation embryo development

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